Mechanisms of Electrical Coupling Between Pyramidal Cells.
Edward J. Vigmond, Jose L. Perez Velazquez, Taufik A. Valiantez, Berj L.
Bardakjiany, Peter L. Carlenz.
Institute of Biomedical Engineering and Department of Electrical & Computer
Engineering, University of Toronto, Playfair Neuroscience Unit and Bloorview
Epilepsy Program, Toronto Hospital - Western Division, University of
Toronto.
APStracts 4:197N, 1997.
ABSTRACT
1. Direct electrical coupling between neurons can be the result of both
electrotonic current transfer through gap junctions and extracellular fields.
Intracellular recordings from CA1 pyramidal neurons of rat hippocampal slices
showed two different types of small amplitude coupling potentials: short
duration (5 ms) biphasic spikelets which resembled differentiated action
potentials, and long duration (>20 ms) monophasic potentials. 2. A three-
dimensional morphological model of a pyramidal cell was employed to determine
the extracellular field produced by a neuron and its effect on a nearby neuron
due to both gap junctional and electric field coupling. Computations were
performed using a novel formulation of the boundary element method which
employs triangular elements to discretize the soma, and cylindrical elements
to discretize the dendrites. An analytic formula was derived to aid in
computations involving cylindrical elements. 3. Simulation results were
compared to biological recordings of intracellular potentials and spikelets.
Field effects produced waveforms resembling spikelets although of smaller mag-
nitude than those recorded in vitro, while gap junctional electrotonic
connections produced waveforms resembling small amplitude excitatory
postsynaptic potentials. 4. Intracellular electrode measurements were found
inadequate for ascertaining membrane events due to externally applied electric
fields. The transmembrane voltage induced by the electric field was highly
spatially dependent in polarity and wave shape as well as being an order of
magnitude larger than activity measured at the electrode. Membrane voltages
due to electrotonic current injection across gap junctions were essentially
constant over the cell and were accurately depicted by the electrode. 5. The
effects of several parameters were investigated (a) decreasing the ratio of
intra- to extra-cellular conductivity reduced the field effects; (b) the tree
structure had a major impact on the intracellular potential; (c) placing the
gap junction in the dendrites introduced a time delay in the gap junctional
mediated electrotonic potential as well as deceasing the potential recorded by
the somatic electrode; (d) field effects decayed to one half their maximum
strength at a cell separation of approximately 20 m. 6. Results indicate that
the in vitro measured spikelets are unlikely to be mediated by gap junctions
and that a spikelet produced by the electric field of a single source cell has
the same waveshape as the measured spikelet but with a much smaller amplitude.
It is hypothesized that spikelets are a manifestation of the simultaneous
electric field effects from several local cells whose action potential firing
is synchronized.
Received 11 Ocotber 1996; accepted in final form 13 August 1997.
APS Manuscript Number J810-6.
Article publication pending J. Neurophysiol.
ISSN 1080-4757 Copyright 1997 The American Physiological Society.
Published in APStracts on 28 August 1997